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Components of the Fiber Diet in the Prevention and Treatment of IBD-An Update.

Katarzyna Ferenc, Sara Jarmakiewicz-Czaja, Rafał Filip
Review Nutrients 2022 19 次引用
PubMed DOI PDF
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Study Design

研究类型
Review
研究人群
IBD patients
干预措施
Components of the Fiber Diet in the Prevention and Treatment of IBD-An Update. None
对照组
None
主要结局
IBD prevention via microbiota modulation
效应方向
Positive
偏倚风险
Unclear

Abstract

Inflammatory bowel disease (IBD) is a group of diseases with a chronic course, characterized by periods of exacerbation and remission. One of the elements that could potentially predispose to IBD is, among others, a low-fiber diet. Dietary fiber has many functions in the human body. One of the most important is its influence on the composition of the intestinal microflora. Intestinal dysbiosis, as well as chronic inflammation that occurs, are hallmarks of IBD. Individual components of dietary fiber, such as β-glucan, pectin, starch, inulin, fructooligosaccharides, or hemicellulose, can significantly affect preventive effects in IBD by modulating the composition of the intestinal microbiota or sealing the intestinal barrier, among other things. The main objective of the review is to provide information on the effects of individual fiber components of the diet on the risk of IBD, including, among other things, altering the composition of the intestinal microbiota.

简要概述

The main objective of the review is to provide information on the effects of individual fiber components of the diet on the risk of IBD, including, among other things, altering the composition of the intestinal microbiota.

Full Text

nutrients

Review

Components of the Fiber Diet in the Prevention and Treatment of IBD—An Update

Katarzyna Ferenc 1 , Sara Jarmakiewicz-Czaja 2 and Rafał Filip 1,3,*

  1. 1 Institute of Medicine, Medical College of Rzeszow University, 35-959 Rzeszow, Poland
  2. 2 Institute of Health Sciences, Medical College of Rzeszow University, 35-959 Rzeszow, Poland
  3. 3 Department of Gastroenterology with IBD Unit, Clinical Hospital No. 2, 35-301 Rzeszow, Poland

* Correspondence: r.s.fi[email protected]

Abstract: Inflammatory bowel disease (IBD) is a group of diseases with a chronic course, characterized by periods of exacerbation and remission. One of the elements that could potentially predispose to IBD is, among others, a low-fiber diet. Dietary fiber has many functions in the human body. One of the most important is its influence on the composition of the intestinal microflora. Intestinal dysbiosis, as well as chronic inflammation that occurs, are hallmarks of IBD. Individual components of dietary fiber, such as β-glucan, pectin, starch, inulin, fructooligosaccharides, or hemicellulose, can significantly affect preventive effects in IBD by modulating the composition of the intestinal microbiota or sealing the intestinal barrier, among other things. The main objective of the review is to provide information on the effects of individual fiber components of the diet on the risk of IBD, including, among other things, altering the composition of the intestinal microbiota.

Keywords: Crohn’s diseases; dietary fiber; inflammatory bowel diseases; nutrition; ulcerative colitis

Citation: Ferenc, K.; Jarmakiewicz-Czaja, S.; Filip, R. Components of the Fiber Diet in the Prevention and Treatment of IBD—An Update. Nutrients 2023, 15,

162. https://doi.org/10.3390/ nu15010162

Academic Editors: Gang Liu and Luna Xu

Copyright: © 2022 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https:// creativecommons.org/licenses/by/ 4.0/).

1. Introduction

Inflammatory bowel diseases (IBDs) are a group of diseases with a chronic course, characterized by periods of exacerbation and remission of the disease. The etiology of IBD is not fully understood; however, many researchers point to a predisposition to the onset of the disease with the existence of certain genetic, environmental, immunological, and microbiological factors [1–3]. IBD can occur in both men and women of all ages. Western lifestyles are causing an increase in the incidence of IBD year after year. Researchers predict that their prevalence will increase significantly in the next few years [4].

A potentially predisposing component to IBD is a Western-type diet, which is, among other things, low in dietary fiber.

Dietary fiber is a broad concept, so different classifications are used to describe it. A division by origin, physicochemical properties, and chemical composition is used [5]. Depending on the solubility of dietary fiber in water, it can be classified as soluble (SDF) and insoluble (IDF). These groups differ in their functionality and mode of action after ingestion [6]. Soluble fiber includes fructooligosaccharides, galactooligosaccharides, pectins, β-glucans and inulin [7]. The second group includes cellulose, hemicellulose, and lignins, among others [8]. Dietary fiber is found in various proportions and in many foods, such as vegetables, fruits, pulses, nuts, seeds, and cereals. However, not all types of fiber are found in the same food groups; pectin is more abundant in fruits and some types of vegetables, and β-glucans are found in cereals [9]. Starchy foods that contain resistant starch include pulses, cereals, and potatoes [10]. Insoluble fiber functions as a means of increasing fecal weight and reducing intestinal transit time, which consequently contributes to relief from constipation [11]. Both soluble and insoluble fibers are indigestible. However, soluble in the presence of water can be quickly and easily fermented by intestinal bacteria into products that act favorably on the intestinal microbiome, mainly short-chain fatty acids (SCFAs) [12]. Therefore, ultimately, it may have some prebiotic functions, but it may also

Nutrients 2023, 15, 162. https://doi.org/10.3390/nu15010162 https://www.mdpi.com/journal/nutrients

positively impact health by reducing the risk of gastrointestinal diseases, such as irritable bowel syndrome (IBS), inflammatory bowel disease (IBD), or constipation [13].

β-glucans are a natural group of polysaccharides consisting of D-glucose monomer units linked by β-glycosidic bonds (1,3, 1,4, 1,6). β-glucans can be found in yeast, fungi, some bacteria, seaweed, and cereals, mainly in oats and barley [14]. The diversity and biological activity of these compounds depend on their molecular structure, the conformation of each polymer, and their solubility [15]. β-glucans from oats have actions typical of dietary fiber through which they improve metabolic health parameters, that is, cholesterol and glucose levels [16,17]. β-glucans from yeast and fungi act as immunomodulators. These compounds work by activating the immune system by initiating the inflammatory process, increasing the response to infections, and through antitumor effects [18]. β-glucans appear to be an interesting option to support drug therapy in various diseases. In this review, we describe current knowledge on the effects of dietary fiber components with special emphasis on disruting the composition of the intestinal microbiota.

2. Influence of Fiber on the Intestinal Microbiota

The intestinal microbiota is all the microorganisms that inhabit the intestines. They include bacteria, viruses, fungi, archaeons, and selected unicellular eukaryotes. On the contrary, the definition of the gut microbiome is the entire collection of genes from microorganisms that reside in the intestines [19]. The human gut microbiome population includes more than 1000 microbial species. The most numerous species are Bacteroidetes and Firmicutes and slightly less numerous are Proteobacteria, Actinobacteria, Verrucomicrobia, Fusobacteria, Cyanobacteria, and others [20]. Most bacteria that live in the intestines are anaerobic microorganisms. The presence of aerobic bacteria has been observed primarily in the cecum.

There are several factors that modulate the composition of the intestinal microbiota. One factor is the use of antibiotics. These are prescription drugs that are often given to children from the first days of life. Due to the dynamic development of the intestinal microbiota in children, it is particularly sensitive to antibiotics. The use of these drugs can affect a decrease in Bifidobacteriaceae and Lactobacillales spp., while it can predispose to an increase in Enterobacteriaceae [21]. In their work, Ianiro et al. point out that the effect of antibiotics on the gut microbiota depends on the type of drug, its dose, and the route of administration, as well as factors that are directly related to humans. However, antibiotic administration can also have a eubiotic effect on the host, that is, it can stimulate the growth of beneficial bacteria [22]. However, the use of this group of drugs is most often associated with the appearance of intestinal dysbiosis, i.e., abnormalities in the composition/function of intestinal microorganisms, which can lead to the development of certain diseases or the appearance of exacerbations [23]. The adverse effects of inadequate antibiotic therapy can also include drug resistance, and thus the development of pathogenic microorganisms and a reduction in the commensal microbiota and its diversity [24].

Another factor that modulates gut microbiota is host genetics [25,26]. The heritability of the microbiome ranges from 2% to 8%. However, the authors of some studies show that environmental factors outweigh the genetic factors responsible for the composition of the host microbiota [27]. In their study, Matsumoto et al. showed, excluding genetic factors, that individual dietary components affect certain bacterial species [28]. Polyphenols, proteins, fats, and dietary fiber are essential components of the metabolic pathways of the intestinal microbiota [29].

There are also scientific reports that highlight the effects of specific types of diet on the intestinal microbiota, so, for example, a vegan diet has a beneficial effect in increasing the number of beneficial microorganisms, while following a low FODMAP diet changes the ratio of Firmicutes to Bacteroidetes and decreases the number of Bifidobacterium [30,31]. Other researchers have also indicated the beneficial effects of a plant-based diet on the gut microbiota [32,33]. Reddel et al. point out that when using low-FODMAP, gluten-free, or ketogenic diets in various pathological conditions, supplementation with selected nutrients

Other researchers have also indicated the beneficial effects of a plant-based diet on the gut microbiota [32,33]. Reddel et al. point out that when using low-FODMAP, gluten-free, or

should be considered, as these diets can significantly exacerbate already existing changes in the gut microbiota [34]. Other authors also point to the effect of age on the composition of the intestinal microbiota [35,36].

nutrients should be considered, as these diets can significantly exacerbate already existing changes in the gut microbiota [34]. Other authors also point to the effect of age on the composition of the intestinal microbiota [35,36].

Dietary fiber has a variety of functions in the human body. One of the most important aspects is its effect on the intestinal microbiome and consequently on the prevention of the occurrence of certain diseases. The utilization of dietary fiber by the intestinal microbiota depends on several factors (Figure 1) [37].

Dietary fiber has a variety of functions in the human body. One of the most important aspects is its effect on the intestinal microbiome and consequently on the prevention of the occurrence of certain diseases. The utilization of dietary fiber by the intestinal microbiota depends on several factors (Figure 1) [37].

Figure 1. Factors affecting fiber utilization by the intestinal microbiota [37]

Dietary fiber, which is only available to the intestinal microbiota, is called MAC (microbiota-accessible carbohydrates). It is mainly a source of energy for the intestinal microbiota. MAC is lower when following a Western-type diet, that is, one with low amounts of dietary fiber. Low MAC can reduce the abundance of some commensal bacterial taxa, which is detrimental to the host [38]. In their work, Usuda et al. indicate that decreased MAC can lead to increased intestinal permeability and the induction of colitis [39]. The reason for this may be a decrease in the production of the receptor agonists of glucagon-like peptide 1 (GLP-1) and glucagon-like peptide 2 (GLP-2), which are required for intestinal regeneration after the appearance of mucosal inflammation [40]. Increasing the MAC may favorably influence the increase in the abundance of Bacteroides thetaiotaomicron, Bifidobacterium spp. [39]. The failure to include dietary fiber can lead to an increase in Clostridium spp., mucinophilic bacteria, and thus increase the risk of inflammation [41]. In turn, a higher content of this dietary component increases the synthesis of SCFA (short chain fatty acids). Myhrstad et al. indicate that this is due to an increase in bacteria such as Ruminococcus, Lachnospira, Akkermannsia, Bifidobacterium, Lactobacillus, and Roseburia [42]. Furthermore, Angelis et al. indicate that it can also reduce the secretion of pro-inflammatory substances, such as trimethylamine N-oxide (low molecular weight uremic toxin), indoxyl sulfate (metabolic product of tryptophan breakdown), and p-cresyl sulfate (product of metabolism of tyrosine and phenylalanine by intestinal bacteria) [29].

Dietary fiber, which is only available to the intestinal microbiota, is called MAC (microbiota-accessible carbohydrates). It is mainly a source of energy for the intestinal microbiota. MAC is lower when following a Western-type diet, that is, one with low amounts of dietary fiber. Low MAC can reduce the abundance of some commensal bacterial taxa, which is detrimental to the host [38]. In their work, Usuda et al. indicate that decreased MAC can lead to increased intestinal permeability and the induction of colitis [39]. The reason for this may be a decrease in the production of the receptor agonists of glucagon-like peptide 1 (GLP-1) and glucagon-like peptide 2 (GLP-2), which are required for intestinal regeneration after the appearance of mucosal inflammation [40]. Increasing the MAC may favorably influence the increase in the abundance of Bacteroides thetaiotaomicron, Bifidobacterium spp. [39]. The failure to include dietary fiber can lead to an increase in Clostridium spp., mucinophilic bacteria, and thus increase the risk of inflammation [41]. In turn, a higher content of this dietary component increases the synthesis of SCFA (short chain fatty acids). Myhrstad et al. indicate that this is due to an increase in bacteria such as Ruminococcus, Lachnospira, Akkermannsia, Bifidobacterium, Lactobacillus, and Roseburia [42]. Furthermore, Angelis et al. indicate that it can also reduce the secretion of pro-inflammatory substances, such as trimethylamine N-oxide (low molecular weight uremic toxin), indoxyl sulfate (metabolic product of tryptophan breakdown), and pcresyl sulfate (product of metabolism of tyrosine and phenylalanine by intestinal bacteria) [29].

Adequate mucus production is essential to maintain complete intestinal health. Dietary fiber has the ability to stimulate the intestinal epithelium to secrete mucus through a mechanical action on the epithelium. Acetate, butyrate, and propionate, which belong to the SCFA group, show the ability to regulate pH in the intestinal lumen and are essential for the supply of energy to enterocytes [43]. In addition, they affect the production of mucus in the intestines. Propionate can be synthesized through three different pathways by intestinal bacteria that reside in the human gut: the acrylate, propanediol, and succinate

pathways, with succinate being the most common. Butyrate is synthesized from two molecules, the latter of which is CoA-transferase in the presence of acetate, which is essential for efficient synthesis of the compound. On the other hand, acetate production occurs from acetyl-coenzyme A through acetyl-CoA to produce the substance [44–46]. Increasing the amount of dietary fiber in the daily diet predisposes to increased amounts of Lactobacillus spp. and Bifidobacterium. This is mainly due to an increase in the intake of fructans and galactooligosaccharides [47]. In a study by Fischer et al. in animal models, it was shown that indirectly through adequate fiber, the intestinal microflora containing A. finegoldii, among others, showed that increased intestinal expression of IL-22. IL-22 is responsible, among other things, for maintaining adequate intestinal barrier function due to the separation of microorganisms from the intestinal epithelium [48]. A high-fiber diet also reduces pro-inflammatory cytokines [49].

The soluble fraction of dietary fiber is used by intestinal microbes to obtain energy through its breakdown into oligosaccharides/monosaccharides [50]. The soluble fraction of dietary fiber includes β-glucans, which are increasingly being studied for their effects on the intestinal microbiome [51]. These polymers composed of D-glucose linked by a β-glycosidic bond show the ability to decrease Enterobacteriaceae, while increasing Bifidobacteria and Lactobacilli [50]. In their study, Wang et al. indicate that β-glucan has the ability to modulate intestinal microflora; however, this depends on its molecular weight. The authors note that for microflora modulation, the use would be to introduce a compound of high molecular weight, since supplementation with 3 g of high-molecular-weight β-glucan increased Bacteroidetes, while it decreased Firmicutes, although diets with 3 g of supplementation per day and 5 g of low molecular weight β-glucan did not change the composition of the intestinal microflora [52]. Carlson et al. analyzed the fermentation of various prebiotics, including β-glucan. They showed that β-glucan and oatmeal containing 28% β-glucan had a significant increase in propionate concentration compared to other compounds they studied (Xyloligosaccharide (XOS) and Inulin, a mixture of dried chicory root containing inulin, pectin, hemi/cellulose) [53]. In another study, the researchers compared the fecal microbiota and metabolomics after a 2-month intervention using 3 g of barley β-glucans. They showed a significant increase in SCFA such as acetic, 2-methylpropanoic, propionic, and butyric acids, suggesting modulation of the composition and metabolic pathways of the intestinal microbiota [54].

Intestinal dysbiosis is one of the features attributed to IBD. It is characterized by a decrease in microbial diversity, an increase in unfavorable pathogenic bacteria, and a decrease in beneficial anaerobic bacteria [55]. Patients with IBD patients show a decrease in the number of bacteria, mainly Firmicutes, while an increase in the population of Proteobacteria. There is a lack of information on whether intestinal dysbiosis in IBD is the cause or one of the consequences of the disease [56]. Intestinal dysbiosis and the associated loss of bacterial diversity can lead to the loss of key functions of the normal intestinal barrier. The result can be a dysregulation of the immune system. These dysfunctions can potentially cause inflammation and a stimulated immune response. As a result, they can contribute to IBD [57]. The fermentation of dietary fiber promotes the formation of short-chain fatty acids (SCFA). These acids have anti-inflammatory effects that protect the intestinal epithelium. One of the bacteria that produce SCFA is F. prauznitzii. Interestingly, a study shows that a lower percentage of these bacteria in the ileum of CD patients is associated with endoscopic recurrence after a period of 6 months. Sokol et al. propose the use of F prausnitzii as a potential probiotic for the treatment of CD [58]. Chiba reports that the amount of F. prausnitzii in CD patients is significantly lower than in healthy individuals. He suggests that a diet rich in fiber does not harm but supports and benefits CD patients [59]. The breakdown of fiber in SCFA by intestinal microbes contributes to a favorable regulation of the intestinal microbiome [60]. Interestingly, it seems that CD patients have a much more pronounced intestinal dysbiosis compared to UC. Lower microbial diversity and poorer stability are observed. Even in the context of the microbiome, CD and UC are distinct disease entities at the microbiome level [61]. UC patients have been found to have a reduced number of

butyrate-producing bacteria R. intestinalis and F. prausnitzii. This appears to be strongly correlated with reduced SCFA in patients with UC [62]. Patients with CD showed an increase in Ruminococcus gnavus and a decrease in F. prausnitzii, Bifidobacterium adolescentis, Dialister invisus, and other bacteria that produce butyrates in stool samples. These findings encourage researchers to further investigate the use of SCFA as a complementary treatment for patients with IBD [63]. Currently, the analysis of the gut microbiota has led researchers to the possibility of using microflora transplants as a therapeutic modality for patients with IBD [64].

Component Biological Role

Reduction of CRP (C reactive protein) in patients with UC (ulcerative colitis). Improvement in gastrointestinal symptoms in patients taking mesalazine. Control of lipid and carbohydrate metabolism. Reduction of pro-inflammatory cytokine production. Modulation of the intestinal microbiota.

β-glucan

Pectin Preventive effect of IBD (inflammatory bowel diseases).

Maintain clinical remission in patients with IBD. Reduction of symptoms associated with active disease. Increase in the production of SCFA (short-chain fatty acids) production. Reduction of inflammation in the colon. Reduction of harmful bacteria.

Starch

Positive effect on the intestinal microbiota by increasing Bifidobacteria. Reduction of inflammation. Decrease in fecal calprotectin concentration. Alleviation of dyspeptic symptoms. Indirect production of SCFAs. Potential immunomodulator in IBD.

Inulin

Growth of fecal Bifidobacteria. Reduction of inflammation, indirectly affecting the reduction of anorexia and weight loss Reduction in the Harvey–Bradshaw index. Improving quality of life by reducing pain and improving stool consistency. Promoting the healing of the intestinal epithelium.

Fructooligosaccharides

Reduction of inflammation in the intestines. Assist in the reconstruction of the intestinal epithelium. Increase the production of butyric acid and acetic acid. Increasing the number of bifidobacteria and eubacteria. Reduction in the level of clinical activity of patients with UC.

Hemicellulose

Intake of fiber in the diet provides many health benefits. Natural sources of fiber contribute minerals, vitamins, water, and a variety of phytonutrients. However, dietary fiber is not only natural food sources but also dietary supplements. According to the latest guidelines, fiber supplementation is indicated as first-line treatment for chronic constipation [131]. One of the studies shows that fiber supplementation effectively relieves constipation. In particular, psyllium, doses > 10 g/d, and treatment durations of at least 4 weeks seem optimal, although caution should be exercised in interpreting the results due to the significant heterogeneity of the study group [132].

Fiber supplements can play an important role in helping fiber intake reach recommended guidance levels. The available clinical trial data suggest that the use of fiber supplements is more effective than the use of high-fiber foods to improve serum lipoprotein

values, improve weight loss, and improve gastrointestinal function. This may be due to the fact that it is easier to use tablets or powders as a secondary source of fiber than to implement proper eating practices [133]. A study indicates that whole-fiber high-fiber diet interventions resulted in more beneficial microbiome outcomes compared to low-fiber diets and fiber supplements [134]. Fiber supplementation causes moderate gastrointestinal side effects, such as flatulence, bloating, diarrhea, and abdominal discomfort, which were significantly higher with fiber supplementation compared to placebo. A review suggests that medical workers should continue to recommend that their patients eat high-fiber foods, such as fruits, vegetables, whole grains, and nuts. Possibly supplement their diet with functional fibers, such as psyllium or β-glucan. This is especially relevant as the mean dietary fiber intake by adults in the USA, it is only 17 g/d, which is clearly under the recommendation of 14 g/1000 kcal or 25 to 38 g/d, as recommended by the National Academy of Medicine [135].

4. Limitations

A limitation of the review may be that there are too few human and animal studies on the effects of selected components of dietary fiber on specific bacterial strains in intestinal microflora and on the effects of individual components in exacerbation and in remission in patients with IBD. Additionally, studies very often lack homogeneous groups of patients in terms of gender, age, or drugs used. However, in the above review, we selected the most reliable research and articles.

5. Summary

Due to one of the etiological factors of IBD, which is the alteration of the intestinal microbiota, care must be taken to ensure an adequate diet, both during the exacerbation and remission of the disease. One of the main dietary components that have a beneficial effect on the intestinal microbiota is dietary fiber. As a result of the range of action of this component, it is divided into insoluble and soluble. Increasingly, researchers are focusing on studying specific components of dietary fiber—β-glucan, pectin, starch, inulin, fructooligosaccharides, or hemicellulose—due to their individual effects in the context of IBD. Dietary fiber has been suggested to be important in the prevention of IBD by reducing pro-inflammatory cytokines, modulating the intestinal microbiota, and reducing gastrointestinal side effects. The introduction of dietary fiber in patients with IBD in remission or exacerbation should be individualized according to the individual needs and digestive capacity of the body. However, research on the properties of various components of dietary fiber and their therapeutic potential is still ongoing.

Author Contributions: Conceptualization, K.F., S.J.-C. and R.F.; writing—original draft preparation, K.F., S.J.-C. and R.F.; writing—review and editing, K.F., S.J.-C. and R.F. All authors have read and agreed to the published version of the manuscript.

Funding: This research did not receive external funding. Data Availability Statement: Not applicable. Conflicts of Interest: The authors declare no conflict of interest.

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